Revision of Meiodorvillea Jumars, 1974 (Annelida: Dorvilleidae) including descriptions of three new species from the Southwestern Atlantic Ocean

Meiodorvillea Jumars, 1974 is a little-known genus of Dorvilleidae Chamberlin, 1919, characterized by its small size and reduced appendages and jaw apparatus. A revision of the genus is presented, including analysis of the type material of M. minuta (Hartman, 1965) and M. apalpata Jumars, 1974, as well as specimens collected from shelf and slope continental areas in Brazil. A neotype was designated for M. minuta and its distribution was extended to Brazil. The identity of M. chilensis (Hartmann-Schröder, 1965) is questioned and three new species from 21 to 1,300.7 meters depth are also described. Meiodorvillea penhae sp. nov. has furcate chaeta only in the first anterior chaetigers. In contrast, Meiodorvillea hartmanae sp. nov. has very small palps and asymmetrical thin furcate chaeta and Meiodorvillea jumarsi sp. nov. has dorsal cirri and geniculate chaeta only in the first anterior chaetigers.


Introduction
The family Dorvilleidae Chamberlin, 1919 [1] currently comprises 32 genera and about 200 species [2]. Among them, 75 belong to Ophryotrocha Claparède & Mecznikow, 1869 [3], of which 35 have been described in the last twenty years [4]. Dorvilleidae includes some of the smallest annelids and shows great morphological heterogeneity, being the only extant family of Eunicida with ctenognath-type jaw apparatus, which consists of two or four rows of symmetrical or subsymmetrical denticulate maxillary plates, upper comb-like jaws, and an unpaired posterior carrier-like structure [2].
Meiodorvillea is composed of very small and simple-bodied species reaching few centimeters in length and few morphological structures for identification. The genus was erected by Jumars [17] to include M. minuta (Hartman, 1965) [13], M. chilensis (Hartmann-Schröder, 1965) [18], and M. apalpata Jumars, 1974 [17]. Meiodorvillea differs from Protodorvillea in the extreme reduction of palps and maxillary apparatus with two rows of maxillary plates or "denticles". Meiodorvillea minuta was described from New England (USA) and M. apalpata from San Diego (USA). Meiodorvillea chilensis is known only from the original description, based on a single specimen from Golfo de Ancud, Chile. Two unnamed species are described by Wolf [19], from Gulf of Mexico (Florida and Texas, USA). Meiodorvillea is a little-known genus with studies restricted to original taxonomic descriptions of species, in addition to Jumars [17], when the genus was erected. It occurs from 21 to 1300 meters depth, lacking adequately fixed samples for molecular studies, and rare in scientific collections, so that its diversity is currently underestimated. In this scenario, relevant studies on the taxonomy, morphology, ecology, biology, ontogeny, and behavior, among others, are absent, leading most specimens from museums to be identified either as Meiodorvillea sp. or as M. minuta.
This study intends to review morphologically the genus Meiodorvillea by designating a neotype for M. minuta and by describing three new species, extending the occurrence of the genus to Brazil. Some morphological characters used in the taxonomy of the genus, as well as its worldwide distribution, are also discussed.

Sampling
Specimens were collected along the Southwestern Atlantic Ocean during two major Brazilian oceanographic research projects carried out between 2008 and 2012, in soft-bottoms from 12 to 3.301 m depth: the Assessment of the Environmental Heterogeneity of the Campos Basin (HABITATS) [20] and the Environmental Characterization of the Espírito Santo Basin (AMBES). The collected specimens were fixed in 4% formalin and preserved in 70% ethanol.

Morphological analysis
The whole body and parapodia from anterior, median and posterior regions of specimens were analyzed under both Zeiss SteREO Discovery V.2.0 and Zeiss Axioskop 2 Plus optical microscopes, and scanning electron microscope (SEM), model JEOL JSM-5800 LV at the Laboratório de Microscopia Eletrônica, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP). Specimens for SEM were immersed 15 minutes in increasing concentrations of ethanol (80, 90, and 95%), followed by 15,30, and 60 minutes in absolute ethanol. Critical point drying (Balzers CPD-30) was carried out at 37˚C and 70 bars, followed by gold coating (Sputter Coater SPD-050) [21]. Jaw apparatuses were prepared for optical microscopy using three methods. 1. Cutting anterior end with about four chaetigers, whitening with 10% KOH (potassium hydroxide) for one to two hours, depending on the specimen size, and mounting on slides with glycerin. 2. Cutting anterior end with about four chaetigers and dissolving the soft tissues with 30% NaClO (sodium hypochlorite), then washing until degradation, and mounting on slides with Hoyer (trichloroacetaldehyde) or Aquatex1. 3. Drying entire specimens on slides and observing by transparency. Jaw apparatuses of the three new species were analyzed and described on nontype specimens, to avoid harming holotypes' integrity. Drawings were made with camera lucida and photos with ZEISS AxioCam MRc, both attached to optical microscope.
Type and some non-type specimens of M. minuta and M. apalpata from the Polychaete Collection (LACM-AHF Poly) of the Natural History Museum of Los Angeles County (NHMLAC) and the Polychaeta Collection (USNM) of the National Museum of Natural History of Smithsonian Institution were not dissected, neither used for SEM, to avoid damaging. The specimens of the new species and M. minuta from Brazil are deposited at the Polychaeta Collection (ZUEC-POL) of the Museu de Diversidade Biológica (MDBio), Instituto de Biologia, Universidade Estadual de Campinas (IB/UNICAMP), São Paulo, Brazil.

Nomenclatural acts
The electronic edition of this article conforms to the requirements of the amended International Code of Zoological Nomenclature, and hence the new names contained herein are available under that Code from the electronic edition of this article. This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix "http://zoobank.org/". The LSID for this publication is: urn:lsid:zoobank.org:pub:D969E420-552D-41DC-9FEB-A5131142E9F7. The electronic edition of this work was published in a journal with an ISSN, and has been archived and is available from the following digital repositories: PubMed Central, LOCKSS and Repositório da Produção Científica e Intelectual da UNICAMP.

Remarks. Jumars
Eibye-Jacobsen & Kristensen [23] proposed the erection of a new genus to M. apalpata, suggesting that it could be a sister group of Meiodorvillea sensu stricto. However, Jumars [17] stated that no 'free denticles' (maxillary plates) remained in the specimens, which did not allow distinguishing a real absence from a handling artifact. Therefore, maxillary plates could be present, but this could not be assessed in handled specimens. Although M. apalpata is the only one with lacking palps, it shares characters, such as absence of dorsal cirri, shape of mandibles, absence of denticles on its anterior margin, and presence of maxillary carrier-like structures. Furthermore, the absence of furcate chaeta is also verified in other species, either in the anterior or posterior region. As proposed by Wolf [19], our analysis found no significant morphological differences to support the erection of the new genus proposed by Eibye-Jacobsen & Kristensen [23]. Therefore, M. apalpata should remain within Meiodorvillea until more specimens will be carefully examined, especially regarding the jaw apparatus.
The present revision allowed including new morphological character states in the generic diagnosis, such as presence and shape of geniculate, furcate and cultriform chaetae and details of jaw apparatus.
The posterior peristomial ring frequently covers the anterior ring in specimens where the contraction of the anterior region is markedly visible (Fig 14A and 14B), which apparently demonstrates the presence of one ring (Figs 1C and 3B) [13,17]. Although this is not a diagnostic character, this variation is mentioned in the descriptions as being rather variable and dependent on the state of contraction caused by fixation of the specimens.

Meiodorvillea minuta (Hartman, 1965)
Designation of neotype. Hartman [13] listed the material examined of M. minuta as 'Records: C 1 (3); S1 3 (11, TYPE); S1 4 (6); D 1 (4)', mentioning off New England as the type locality, but not designating holotype and paratypes. Jumars [17] mentioned and re-examined the holotype, without clarifying the exact type locality.  The catalog of the Polychaete Collection of the Natural History Museum of Los Angeles County (NHMLAC) has registered the holotype, examined by Jumars [17], in the lot LAC-M-AHF Poly 0691 and seven paratypes in LACM-AHF Poly 0692. Both lots were assigned later the Hartman's [13] publication, the holotype by assistants of Olga Hartman and paratypes by Kristian Fauchald (Leslie Harris, NHMLAC, pers com.), at the time a graduate student, but who has become one of the greatest 20th century polychaetologists. Although Jumars [17] examined and described the holotype, the vial was empty, so that the holotype is missing.
Both R/V Atlantis Expedition Gay Head (Bermuda Transect)'s data [13] and the NHMLAC's catalog show that the type locality of M. minuta is the Station Sl 3 (letter 'l', instead number '1'), meaning Station Slope 3 (east of upper end of Block Canyon, in New England upper continental slope), at 39˚58'24"N, 70˚40'18"W, 300 meters deep, collected at 28 August 1962. Thus, in accordance with ICZN's Articles 75.1 and 75.3.1 [28], we designate the neotype LACM-AHF Poly 12561, selected from the paratypes of LACM-AHF Poly 0692, clarifying the type locality of M. minuta.
In the same way, considering Articles 75.3.2 and 75.3.3 of the ICZN [28], the neotype is named to ensure morphological data sufficient for recognition of the species, clarifying the correct presence and distribution of dorsal and ventral cirri, not clearly described by Hartman [13] and Jumars [17]. Likewise, M. minuta represents the species type of the genus, requiring the correct registration of its morphological characters.
Prostomium pear-shaped, as long as wide, anterior half depressed, posterior half globular, as long as the first two segments (Fig 1A-1C). Eyes absent. One pair of clavate antennae inserted dorsolaterally on middle posterior half of prostomium, 2/3 of prostomium length.
One pair of small and clavate palps inserted laterally at prostomium base, 1/3 as long as antennae (Fig 1B and 1C). Jaw apparatus not dissected. Mandibles butterfly-shaped medially fused, anterior region enlarged with smooth margins without free or fused teeth, posterior region slender and curved. Basal plates of maxillae with smooth inner margin; two rows of 12-15 pairs of denticulate maxillary plates [17].
Two peristomial rings, posterior wider and longer than anterior, covering it dorsally. Chaetigers wide and short, anterior narrower than median and posterior (Fig 1A).
Cylindrical parapodia, first pair smaller than the following ones, gradually tapering towards posterior region (Fig 1A, 1D and 1E). Small and rounded dorsal cirrus on chaetigers 2 to 9 (Fig 1D), inserted slightly distally on the parapodium, absent thereafter. Small papilliform ventral cirrus in all parapodia, absent in the first one (Fig 1E), inserted medially in the parapodium; ventral cirrus larger than dorsal on same parapodium. Supra-acicular chaetae: (1) one long and serrated capillary (Fig 1F), with a small limb anteriorly, longer and thinner in median and posterior regions; (2) one thick furcate with short triangular prongs, asymmetrical in size and shape and serrated base (Fig 1G), thinner and longer in median and posterior regions. From chaetiger 9, two capillaries and one furcate. Sub-acicular chaetae: (3) three compound heterogomphs (Fig 1H), distal end of shafts serrated and blades unidentate with serrated cutting edge; dorsalmost longest with falcigerous or spinigerous blade, median falcigerous, ventralmost falcigerous and shortest. Cultriform chaeta absent. Chaetae from median and posterior regions longer and slender. One internal thick acicula.
Pygidium rounded and smaller than previous chaetigers. Two pairs of clavate pygidial cirri (Fig 1A), dorsal pair with 1.5 times as long as pygidium, ventral pair as long as the pygidium.
Antennae 1/3-2/3 the length of the prostomium. Some specimens with posterior peristomial ring covering the anterior dorsally. Dorsal cirri from chaetigers 2 to 5-9. Two capillary chaetae in median and posterior regions in most specimens and presence of serrated cultriform chaetae in paratypes and Brazilian specimens, replacing the ventralmost compound ( Fig 5F).
Jaw apparatus of ZUEC-POL specimens with ventrally and medially fused mandibles, anterior region enlarged with smooth margins without free or fused teeth, posterior region slender and curved (Fig 6A). Basal plates of maxillae with smooth inner margin, two subsymmetrical rows with 10-12 pairs of free rectangular and denticulate maxillary plates, each one with one posterior main fang and usually four anterior teeth; anterior and posteriormost plates larger and rounded, with small and more numerous teeth (Fig 6B).
Remarks. Hartman [13] described the parapodial cirri as being obscure and reduced to slight projections in all parapodia, which differs from the analysis performed on the type series and non-type material. The LACM-AHF Poly specimens did not have cirri in parapodium 1, but rather a small papilliform ventral cirrus from the 2, in addition to a small and rounded dorsal cirrus from the parapodia 2 to 7-9. The length of antennae in the original description is not accurate, being actually 2/3 the length of prostomium. The furcate chaetae become slender and longer with asymmetrical prongs in median and posterior regions, character not mentioned by Hartman [13].
The jaw apparatus of the type series was not analyzed, but the morphology of the ZUEC-POL specimens agrees with Jumars's [17] description.

Meiodorvillea apalpata
Jaw apparatus not dissected. Mandibles butterfly-shaped medially fused, anterior region enlarged with smooth margins without free or fused teeth, posterior region slender and curved. Pair of maxillary carrier-like structures relatively large, basal plates with dentate inner margin; maxillary plates absent [17].
Two peristomial rings, both as long as prostomium, clearly well-defined dorsally and ventrally; posterior wider and longer than anterior and almost as long as the following chaetigers (Fig 7A).
Cylindrical parapodia, shorter in anterior, longer and narrower in posterior region. Dorsal cirrus absent. Papilliform ventral cirrus inserted medially in the parapodium, absent in the first one (Fig 7C).
Pygidium rounded and narrower than previous chaetigers. Two pairs of clavate pygidial cirri, dorsal pair as long as pygidium, ventral pair half as long as pygidium (Fig 7B).
Remarks. Although the type material was in poor condition, the following differences from the original description were observed: presence of papilliform ventral cirrus inserted in the middle of the parapodium (Fig 7C), similar to M. minuta; absence of neuroacicula; presence of cultriform chaeta in some specimens, including the holotype.
Jumars [17] did not mention the presence of maxillary plates in the jaw apparatus, although more material is needed to better describe this structure.
Geographic distribution and bathymetric range. Known only from the type locality, Northeastern Pacific Ocean, east coast of California (USA), 1,223-1,224 m, silty mud [17].

Meiodorvillea penhae sp. nov.
(Figs 8-12, Table 1 Diagnosis. One pair of antennae and one pair of palps. Dorsal cirrus absent. Ventral cirrus papilliform, absent in the first chaetiger. Chaetae capillary, furcate thick and symmetrical on chaetigers 1 to 7-9, replaced by geniculate towards the end of body, dorsalmost compound spiniger or falciger, median and ventralmost falcigers, and cultriform in last chaetigers in some specimens, replacing the ventralmost compound. Two pairs of pygidial cirri. Description of the holotype. Complete specimen, 45 chaetigers, 2.2 mm long, 0.21 mm wide in anterior region, 0.14 mm in posterior region, excluding parapodia. Width uniform, anterior region slightly wider (Fig 8A). Color in ethanol pale yellow.

PLOS ONE
Two peristomial rings, both as long as prostomium when not retracted into prostomium (Figs 8B and 9A-9D); posterior wider than anterior, covering it dorsally. Transversal ciliary bands at base of peristomium and anterior chaetigers (Fig 9C).
Jaw apparatus from additional non-type material with ventral and medially fused mandibles, anterior region enlarged with smooth margins without free or fused teeth, posterior region slender and curved (Fig 12A and 12B). Basal plates of maxillae with smooth inner margin, two subsymmetrical rows with 10 to 13 pairs of free rectangular and denticulate maxillary

PLOS ONE
Revision of Meiodorvillea with three new species from Southwestern Atlantic plates, each one with one posterior main fang and usually four anterior teeth, last and anteriormost plates larger and rounded, with small and more numerous teeth. (Fig 12A and 12C).
Remarks. Meiodorvillea penhae sp. nov. has furcate chaeta in anterior region replaced by geniculate in median and posterior regions, differing from any other species of Meiodorvillea, but occurring in Gymnodorvillea floridana Wainright & Perkins, 1982 [31].
The poor condition of the specimens did not allow detecting the possible presence of basal ciliated bands in median and posterior chaetigers.
Meiodorvillea penhae sp. nov. resembles M. minuta in having antennae and palps of same length and as long as the prostomium. However, geniculate chaetae are only present in the former and dorsal cirri only in the latter. Meiodorvillea apalpata differs from both species in lacking palps and furcate chaetae. Meiodorvillea penhae sp. nov. apparently corresponds to morphotypes with rasper-like maxillary plates of Meiodorvillea sp. A, described by Wolf [19].
Geographic distribution and bathymetric range. Southwestern Atlantic Ocean, States of Espírito Santo and Rio de Janeiro (Brazil), 21 to 158 m, in sand, muddy sand, sand with biodetritus, sand with rhodoliths, mud, mud with biodetritus and rhodoliths with mud.
Etymology. The specific epithet "penhae" refers to Our Lady of Penha, patron saint of the State of Espírito Santo.
Prostomium pear-shaped, as long as wide, anterior half depressed and rounded, posterior half wider and globular (Figs 13A, 13B and 14A-14C). Eyes absent. One pair of clavate antennae inserted dorsolaterally on middle posterior half of prostomium, 1/3 of prostomium length (Figs 13B, 13C and 14A-14C). One pair of very small and clavate palps inserted laterally at prostomium base, difficult to see in dorsal view (Figs 13C and 14C).
Jaw apparatus from additional non-type material with ventral and medially fused mandibles, anterior region enlarged with smooth margins without free or fused teeth, posterior region slender and curved (Fig 17A). Basal plates of maxillae with smooth inner margin, two subsymmetrical rows with 10-12 pairs of free rectangular and denticulate maxillary plates, each one with one posterior main fang and usually four anterior teeth last and anteriormost plates larger and rounded, with small and more numerous teeth. (Fig 17A-17C).
Remarks. Meiodorvillea hartmanae sp. nov. resembles M. apalpata and M. penhae in having papilliform ventral cirrus in all parapodia (except the 1 st ), but differs having furcate and lacking geniculate chaetae. On the other hand, M. minuta differs in having dorsal cirri on anterior chaetigers and a different shape of furcate.
Meiodorvillea hartmanae sp. nov. has smaller palps than all other species of the genus. In some specimens the palps are very difficult to see in dorsal view; in others, only ventrally. The species also has remnants of ciliary bands in the prostomium, peristomium, and chaetigers, as M. penhae and M. minuta. This character may possibly be shared by all species of Meiodorvillea. Diagnosis. One pair of antennae and one pair of palps. Dorsal cirrus papilliform from chaetigers 2 to 5-9. Ventral cirrus papilliform, absent in the first chaetiger. Chaetae capillary, geniculate on chaetigers 1 to 7-13, replaced by furcate asymmetrical towards the end of body, dorsalmost compound spiniger or falciger and Y-shaped shafts in the first chaetigers, median and ventralmost falcigers, and cultriform in last chaetigers in some specimens, replacing the ventralmost compound. Two pairs of pygidial cirri.
Description of the holotype. Complete specimen, 39 chaetigers, 2.26 mm long, 0.84 mm wide in anterior region, excluding parapodia; body width uniform, anterior region slightly wider (Fig 18A). Color in ethanol pale yellow.
Two peristomial rings, both as long as the prostomium when not retracted, posterior wider and slightly longer than anterior dorsally (Figs 18B,19A and 19B). Transversal ciliary bands at base of peristomium and anterior chaetigers (Fig 19A).
Pygidium rounded and narrower than previous chaetigers. Two pairs of clavate pygidial cirri, dorsal pair twice as long as pygidium, ventral pair 1.5 times as long as pygidium (Figs 18D,19C and 19D). Jaw apparatus from additional non-type material with ventral and medially fused mandibles, anterior region enlarged with smooth margins without free or fused teeth, posterior region slender and curved (Fig 22A). Basal plates of maxillae with smooth inner margin, two subsymmetrical rows with 10-12 pairs of free rectangular and denticulate maxillary plates, each one with one posterior main fang and usually four anterior teeth, last and anteriormost plates larger and rounded, with small and more numerous teeth. (Fig 22A and 22B).
Remarks. Meiodorvillea jumarsi sp. nov. differs from M. apalpata in having furcate and dorsal papilliform cirrus in anterior parapodia. The latter character also occurs in M. minuta, differing from the new species in lacking geniculate chaetae. Meiodorvillea jumarsi sp. nov. has geniculate chaetae in anterior parapodia replaced by furcate, while M. penhae has furcate replaced by geniculate chaetae in median and posterior regions. Meiodorvillea jumarsi sp. nov. also differs from M. hartmanae in having dorsal cirrus papilliform in anterior parapodia and from Meiodorvillea sp. B [19] in having palps.
Etymology. The specific epithet "jumarsi" honors Peter A. Jumars for his insight contributions to the study of polychaetes and for first describing the genus Meiodorvillea.
A key to species of Meiodorvillea is presented below, as well as the Table 1 provides an overview of the main morphological features.

Discussion
This study provides the first record of Meiodorvillea from the Southwestern Atlantic Ocean, from a highly diverse and important protected area of the Brazilian coast. Our careful observations revealed new external morphological characters related to some appendages (presence and form of dorsal and ventral cirri and palps), chaetae (presence and form of furcate, geniculate and cultriform, as well as details of compound), and presence of ciliary bands, allowing to clarify the distinction between the previously known species, as well as to describe three new species. Conversely, new analyses of the jaw apparatus on a larger number of newly collected specimens are needed to understand this structure in each taxon, especially M. apalpata.
Meiodorvillea species show different bathymetric distributions (Table 1). Meiodorvillea penhae occurs between 21-158 meters depth, limited to continental shelf. Meiodorvillea jumarsi (41-432 meters depth), on the other hand, extends its distribution to slope areas, while M. hartmanae (964.8-1,300.7 m) and M. apalpata (1,223-1224 m) occur in deeper regions of the continental slope. The distribution of M. minuta (97-1050 meters depth) is more extensive, occurring from the continental shelf to deeper slope areas, both in the USA and in Brazil. However, the rare availability of collected material and few studies of this species are barriers to explain its disjoint distribution.
The taxonomy and phylogeny of Dorvilleidae remains unclear due to collecting difficulties, but also to the misclassification and omission of relevant morphological characters, especially from the jaw apparatus, a fundamental structure within Eunicida that, instead, did not show relevant differences among the known species of Meiodorvillea.